Grapevine leafroll disease and associated viruses: a unique pathosystem.

Grapevine leafroll is the most complex and intriguing viral disease of grapevine (Vitis spp.). Several monopartite closteroviruses (family Closteroviridae) from grapevines have been molecularly characterized, yet their role in disease etiology is not completely resolved. Hence, these viruses are currently designated under the umbrella term of Grapevine leafroll-associated viruses (GLRaVs). This review examines our current understanding of the genetically divergent GLRaVs and highlights the emerging picture of several unique aspects of the leafroll disease pathosystem. A systems biology approach using contemporary technologies in molecular biology, -omics, and cell biology aids in exploring the comparative molecular biology of GLRaVs and deciphering the complex network of host-virus-vector interactions to bridge the gap between genomics and phenomics of leafroll disease. In addition, grapevine-infecting closteroviruses have a great potential as designer viruses to pursue functional genomics and for the rational design of novel disease intervention strategies in this agriculturally important perennial fruit crop.

[1]  J. Burgyán,et al.  Viral suppressors of RNA silencing. , 2011, Trends in plant science.

[2]  E. Koonin,et al.  Viral AlkB proteins repair RNA damage by oxidative demethylation , 2008, Nucleic acids research.

[3]  J. Culver,et al.  Virus-induced disease: altering host physiology one interaction at a time. , 2007, Annual review of phytopathology.

[4]  E. Koonin,et al.  Diverse suppressors of RNA silencing enhance agroinfection by a viral replicon. , 2006, Virology.

[5]  F. Mannini,et al.  A multidisciplinary study on the effects of phloem-limited viruses on the agronomical performance and berry quality of Vitis vinifera cv. Nebbiolo. , 2011, Journal of proteomics.

[6]  P. Perata,et al.  Sucrose-Specific Induction of the Anthocyanin Biosynthetic Pathway in Arabidopsis[W] , 2005, Plant Physiology.

[7]  Y. Motomura 14C-Assimilate Partitioning in Grapevine Shoots: Effects of Shoot Pinching, Girdling of Shoot, and Leaf-Halving on Assimilates Partitioning from Leaves into Clusters , 1993, American Journal of Enology and Viticulture.

[8]  G. Martelli DIRECTORY OF VIRUS AND VIRUS-LIKE DISEASES OF THE GRAPEVINE AND THEIR AGENTS , 2014 .

[9]  V. Dolja,et al.  Comparative and functional genomics of closteroviruses , 2006, Virus Research.

[10]  R. Turgeon,et al.  Minor vein structure and sugar transport in Arabidopsis thaliana , 2000, Planta.

[11]  Jungmin Lee,et al.  Influence of grapevine leafroll associated viruses (GLRaV-2 and -3) on the fruit composition of Oregon Vitis vinifera L. cv. Pinot noir: Phenolics , 2009 .

[12]  Vladimir Nekrasov,et al.  Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system , 2013, Plant Methods.

[13]  M. Fuchs,et al.  Tolerance and Resistance to Viruses and Their Vectors in Vitis sp.: A Virologist’s Perspective of the Literature , 2011, American Journal of Enology and Viticulture.

[14]  Damien Afoufa-Bastien,et al.  The Vitis vinifera sugar transporter gene family: phylogenetic overview and macroarray expression profiling , 2010, BMC Plant Biology.

[15]  W. Dawson,et al.  The conserved structures of the 5' nontranslated region of Citrus tristeza virus are involved in replication and virion assembly. , 2003, Virology.

[16]  J. Poulain,et al.  The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla , 2007, Nature.

[17]  N. Killiny,et al.  Citrus tristeza virus-based RNAi in citrus plants induces gene silencing in Diaphorina citri, a phloem-sap sucking insect vector of citrus greening disease (Huanglongbing). , 2014, Journal of biotechnology.

[18]  E. Domingo,et al.  Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. , 1992, Gene.

[19]  Jean-François Martin,et al.  Distinct Viral Populations Differentiate and Evolve Independently in a Single Perennial Host Plant , 2006, Journal of Virology.

[20]  O. Voinnet,et al.  Cell-to-cell and long-distance siRNA movement in plants: mechanisms and biological implications. , 2011, Current opinion in plant biology.

[21]  V. Dolja,et al.  Virion tails of Beet yellows virus: Coordinated assembly by three structural proteins. , 2007, Virology.

[22]  Dustin A. Cartwright,et al.  A High Quality Draft Consensus Sequence of the Genome of a Heterozygous Grapevine Variety , 2007, PloS one.

[23]  Charles W. Melnyk,et al.  Silencing signals in plants: a long journey for small RNAs , 2011, Genome Biology.

[24]  W. Dawson,et al.  Closterovirus bipolar virion: evidence for initiation of assembly by minor coat protein and its restriction to the genomic RNA 5' region. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[25]  D. J. Lewandowski,et al.  An engineered closterovirus RNA replicon and analysis of heterologous terminal sequences for replication. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  J. García,et al.  How do plant viruses induce disease? Interactions and interference with host components. , 2011, The Journal of general virology.

[27]  Michael A. McCarthy,et al.  Dynamics of grape berry growth and physiology of ripening. , 2000 .

[28]  S. Somerville,et al.  Senescence-associated genes induced during compatible viral interactions with grapevine and Arabidopsis. , 2007, Journal of experimental botany.

[29]  V. Dolja,et al.  Genetic analysis of the cell-to-cell movement of beet yellows closterovirus. , 2000, Virology.

[30]  Jungmin Lee,et al.  Influence of grapevine leafroll associated viruses (GLRaV-2 and -3) on the fruit composition of Oregon Vitis vinifera L. cv. Pinot noir: Free amino acids, sugars, and organic acids , 2009 .

[31]  L. Miozzi,et al.  Genome-wide identification of viral and host transcripts targeted by viral siRNAs in Vitis vinifera. , 2013, Molecular plant pathology.

[32]  D. Golino,et al.  A putative new ampelovirus associated with grapevine leafroll disease , 2010, Archives of Virology.

[33]  S. Elena,et al.  A Viral Protein Mediates Superinfection Exclusion at the Whole-Organism Level but Is Not Required for Exclusion at the Cellular Level , 2014, Journal of Virology.

[34]  Rodrigo P. P. Almeida,et al.  Ecology and management of grapevine leafroll disease , 2013, Front. Microbiol..

[35]  E. Domingo,et al.  Viruses as Quasispecies: Biological Implications , 2006, Current topics in microbiology and immunology.

[36]  R. Naidu,et al.  High-throughput sequence analysis of small RNAs in grapevine (Vitis vinifera L.) affected by grapevine leafroll disease. , 2012, Molecular plant pathology.

[37]  T. Lacombe,et al.  Historical origins and genetic diversity of wine grapes. , 2006, Trends in genetics : TIG.

[38]  S. Elena,et al.  A systems biology approach to the evolution of plant-virus interactions. , 2011, Current opinion in plant biology.

[39]  D. Huson,et al.  Application of phylogenetic networks in evolutionary studies. , 2006, Molecular biology and evolution.

[40]  J. Lousada,et al.  Impacts of leafroll‐associated viruses (GLRaV‐1 and ‐3) on the physiology of the Portuguese grapevine cultivar ‘Touriga Nacional’ growing under field conditions , 2012 .

[41]  B. Holzapfel,et al.  Sugars and flowering in the grapevine (Vitis vinifera L.). , 2008, Journal of experimental botany.

[42]  B. Falk,et al.  Lettuce infectious yellows virus: in vitro acquisition analysis using partially purified virions and the whitefly Bemisia tabaci. , 1999, The Journal of general virology.

[43]  S. Namba,et al.  Grapevine Leafroll Virus, a Possible Member of Closteroviruses , 1979 .

[44]  A. Schilder,et al.  Effects of grapevine leafroll associated virus 3 infection on growth, leaf gas exchange, yield and basic fruit chemistry of Vitis vinifera L. cv. Cabernet Franc , 2014 .

[45]  M. Barón,et al.  Inhibition of photosynthesis by viral infection : Effect on PSII structure and function , 2000 .

[46]  M. Daugherty,et al.  Seasonal dynamics and virus translocation of Grapevine leafroll-associated virus 3 in grapevine cultivars , 2012 .

[47]  S. Duffy,et al.  A divergent variant of Grapevine leafroll-associated virus 3 is present in California , 2012, Virology Journal.

[48]  P. Gugerli,et al.  Genome organization, serology and phylogeny of Grapevine leafroll-associated viruses 4 and 6: taxonomic implications. , 2012, Virus research.

[49]  Hironori Kobayashi,et al.  Pink-Colored Grape Berry Is the Result of Short Insertion in Intron of Color Regulatory Gene , 2011, PloS one.

[50]  D. Braun SWEET! The Pathway Is Complete , 2012, Science.

[51]  J. Burger,et al.  MicroRNAs in fruit trees: discovery, diversity and future research directions. , 2014, Plant biology.

[52]  G. Gale Saving the vine from Phylloxera: a never-ending battle , 2002 .

[53]  W. Dawson,et al.  Virus-based transient expression vectors for woody crops: a new frontier for vector design and use. , 2013, Annual review of phytopathology.

[54]  R. Naidu,et al.  3'-coterminal subgenomic RNAs and putative cis-acting elements of Grapevine leafroll-associated virus 3 reveals 'unique' features of gene expression strategy in the genus Ampelovirus , 2010, Virology Journal.

[55]  S. Whitham,et al.  Global impact: elucidating plant responses to viral infection. , 2006, Molecular plant-microbe interactions : MPMI.

[56]  J. Burger,et al.  Complete nucleotide sequence of a South African isolate of grapevine leafroll-associated virus 3 reveals a 5′UTR of 737 nucleotides , 2008, Archives of Virology.

[57]  M. Axtell Classification and comparison of small RNAs from plants. , 2013, Annual review of plant biology.

[58]  Timothy E. Martinson,et al.  Economic Impact of Grapevine Leafroll Disease on Vitis vinifera cv. Cabernet franc in Finger Lakes Vineyards of New York , 2012, American Journal of Enology and Viticulture.

[59]  O. Postnikova,et al.  Comparative analysis of microarray data in Arabidopsis transcriptome during compatible interactions with plant viruses , 2012, Virology Journal.

[60]  Shou-Wei Ding,et al.  Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[61]  V. Dolja,et al.  Complex molecular architecture of beet yellows virus particles. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Edward S. Buckler,et al.  Genetic structure and domestication history of the grape , 2011, Proceedings of the National Academy of Sciences.

[63]  D. Šafářová,et al.  Photosynthetic alterations of pea leaves infected systemically by pea enation mosaic virus: A coordinated decrease in efficiencies of CO(2) assimilation and photosystem II photochemistry. , 2011, Plant physiology and biochemistry : PPB.

[64]  V. Dolja,et al.  HSP70 homolog functions in cell-to-cell movement of a plant virus. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[65]  D. Huson,et al.  Improved Layout of Phylogenetic Networks , 2008, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[66]  N. A. Miroshnichenko,et al.  Virion RNA of beet yellows closterovirus: cell-free translation and some properties , 1989 .

[67]  L. Tian,et al.  Sugars induce anthocyanin accumulation and flavanone 3-hydroxylase expression in grape berries , 2009, Plant Growth Regulation.

[68]  V. Dolja,et al.  Tandem leader proteases of Grapevine leafroll-associated virus-2: Host-specific functions in the infection cycle , 2008, Virology.

[69]  J. Burger,et al.  Mapping of the 5' terminal nucleotides of Grapevine leafroll-associated virus 3 sgRNAs. , 2010, Virus research.

[70]  James F Harbertson,et al.  Modulation of flavonoid biosynthetic pathway genes and anthocyanins due to virus infection in grapevine (Vitis vinifera L.) leaves , 2010, BMC Plant Biology.

[71]  Xianbing Wang,et al.  Virus infection triggers widespread silencing of host genes by a distinct class of endogenous siRNAs in Arabidopsis , 2014, Proceedings of the National Academy of Sciences.

[72]  Rodrigo P. P. Almeida,et al.  Grapevine leafroll-associated virus 3 , 2013, Front. Microbiol..

[73]  Ying-Bo Mao,et al.  Interaction between Two Timing MicroRNAs Controls Trichome Distribution in Arabidopsis , 2014, PLoS genetics.

[74]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[75]  R. Naidu,et al.  Molecular characterization and impacts of a strain of Grapevine leafroll-associated virus 2 causing asymptomatic infection in a wine grape cultivar , 2013, Virology Journal.

[76]  J. Syller Biological and molecular events associated with simultaneous transmission of plant viruses by invertebrate and fungal vectors. , 2014, Molecular plant pathology.

[77]  D. Rees,et al.  High-throughput sequencing reveals small RNAs involved in ASGV infection , 2014, BMC Genomics.

[78]  V. Dolja,et al.  Movement Protein of a Closterovirus Is a Type III Integral Transmembrane Protein Localized to the EndoplasmicReticulum , 2004, Journal of Virology.

[79]  J. Burger,et al.  Three genetic grapevine leafroll-associated virus 3 variants identified from South African vineyards show high variability in their 5′UTR , 2010, Archives of Virology.

[80]  E. Koonin,et al.  The closterovirus-derived gene expression and RNA interference vectors as tools for research and plant biotechnology , 2013, Front. Microbiol..

[81]  L. Miozzi,et al.  Deep sequencing analysis of viral short RNAs from an infected Pinot Noir grapevine. , 2010, Virology.

[82]  Da-Peng Zhang,et al.  A Shift of Phloem Unloading from Symplasmic to Apoplasmic Pathway Is Involved in Developmental Onset of Ripening in Grape Berry1 , 2006, Plant Physiology.

[83]  Manuele Bicego,et al.  The Grapevine Expression Atlas Reveals a Deep Transcriptome Shift Driving the Entire Plant into a Maturation Program[W][OA] , 2012, Plant Cell.

[84]  V. Dolja,et al.  The family Closteroviridae revised , 2002, Archives of Virology.

[85]  A. Karasev Genetic Diversity and Evolution of Closteroviruses. , 2000, Annual review of phytopathology.

[86]  G. Martelli,et al.  Major graft-transmissible diseases of grapevines: nature, diagnosis, and sanitation , 2001 .

[87]  S. Cowell,et al.  Differential tropism in roots and shoots infected by Citrus tristeza virus. , 2014, Virology.

[88]  V. Dolja,et al.  Suppressor of RNA silencing encoded by Beet yellows virus. , 2003, Virology.

[89]  J. Flexas,et al.  Analysis of the virus-induced inhibition of photosynthesis in malmsey grapevines. , 2003, The New phytologist.

[90]  D. Rees,et al.  Phylogenomic Analysis Reveals Deep Divergence and Recombination in an Economically Important Grapevine Virus , 2015, PloS one.

[91]  R. Mittler,et al.  Abiotic stress, the field environment and stress combination. , 2006, Trends in plant science.

[92]  Paul K. Boss,et al.  New insights into grapevine flowering. , 2003, Functional plant biology : FPB.

[93]  J. Burger,et al.  Complete nucleotide sequence of a new strain of grapevine leafroll-associated virus 3 in South Africa , 2012, Archives of Virology.

[94]  E. Koonin,et al.  Genomic and biological analysis of Grapevine leafroll-associated virus 7 reveals a possible new genus within the family Closteroviridae. , 2012, Virus research.

[95]  D. Golino,et al.  Mealybug transmission of Grapevine leafroll viruses: an analysis of virus-vector specificity. , 2010, Phytopathology.

[96]  Varvara I. Maliogka,et al.  TAXONOMIC REVISION OF THE FAMILY CLOSTEROVIRIDAE WITH SPECIAL REFERENCE TO THE GRAPEVINE LEAFROLL-ASSOCIATED MEMBERS OF THE GENUS AMPELOVIRUS AND THE PUTATIVE SPECIES UNASSIGNED TO THE FAMILY , 2012 .

[97]  J. Ng,et al.  A virus capsid component mediates virion retention and transmission by its insect vector , 2011, Proceedings of the National Academy of Sciences.

[98]  R. Turgeon,et al.  Phloem transport: cellular pathways and molecular trafficking. , 2009, Annual review of plant biology.

[99]  M. Thomas,et al.  A molecular genetic perspective of reproductive development in grapevine. , 2008, Journal of experimental botany.

[100]  Z. Yin,et al.  Alteration of host-encoded miRNAs in virus infected plants—experimentally verified , 2014 .

[101]  V. Dolja,et al.  Virus-Derived Gene Expression and RNA Interference Vector for Grapevine , 2012, Journal of Virology.

[102]  J. Hunter,et al.  Distribution of 14C-Photosynthetate in the Shoot of Vitis vinifera L. cv Cabernet Sauvignon I. The Effect of Leaf Position and Developmental Stage of the Vine , 2017 .

[103]  O. Voinnet,et al.  RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence , 2013, Nature Reviews Microbiology.

[104]  The p19.7 RNA silencing suppressor from Grapevine leafroll-associated virus 3 shows different levels of activity across phylogenetic groups , 2012, Virus Genes.

[105]  G. Martelli,et al.  Ultrastructure of grapevine leafroll-associated virus 2 and 7 infections. , 2000 .

[106]  M. Thomas,et al.  White grapes arose through the mutation of two similar and adjacent regulatory genes. , 2007, The Plant journal : for cell and molecular biology.

[107]  Olivier Voinnet,et al.  The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. , 2014, Annual review of plant biology.

[108]  J. G. Charles,et al.  A review of the ecology of grapevine leafroll associated virus type 3 (GLRaV-3) , 2006 .

[109]  T. Lacombe,et al.  Genetic structure in cultivated grapevines is linked to geography and human selection , 2013, BMC Plant Biology.

[110]  R. Naidu,et al.  Grapevine leafroll-associated virus 1 occurs as genetically diverse populations. , 2011, Phytopathology.

[111]  V. Dolja,et al.  Interaction between Long-Distance Transport Factor and Hsp70-Related Movement Protein of Beet Yellows Virus , 2002, Journal of Virology.

[112]  S. Moxon,et al.  Deep Sequencing of Viroid-Derived Small RNAs from Grapevine Provides New Insights on the Role of RNA Silencing in Plant-Viroid Interaction , 2009, PloS one.

[113]  J. T. Matus,et al.  Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes , 2008, BMC Plant Biology.

[114]  N. Nedunchezhian,et al.  Effect of Grapevine Leafroll on the Photosynthesis of Field Grown Grapevine Plants (Vitis vinifera L. cv. Lagrein) , 2004 .

[115]  J. Syller Facilitative and antagonistic interactions between plant viruses in mixed infections. , 2012, Molecular plant pathology.

[116]  R. Naidu,et al.  Grapevine Leafroll: A Complex Viral Disease Affecting a High-Value Fruit Crop. , 2014, Plant disease.

[117]  S. Delrot,et al.  An update on sugar transport and signalling in grapevine. , 2014, Journal of experimental botany.

[118]  R. Naidu,et al.  Genetic variability of natural populations of Grapevine leafroll-associated virus 2 in Pacific Northwest vineyards. , 2010, Phytopathology.

[119]  W. Dawson,et al.  Exploring the limits of vector construction based on Citrus tristeza virus. , 2014, Virology.

[120]  Alain Bouquet,et al.  Biology of the Grapevine , 1992 .

[121]  N. Nedunchezhian,et al.  Leaf age effects on chlorophyll, Rubisco, photosynthetic electron transport activities and thylakoid membrane protein in field grown grapevine leaves , 2002 .

[122]  B. Falk,et al.  Virus-vector interactions mediating nonpersistent and semipersistent transmission of plant viruses. , 2006, Annual review of phytopathology.

[123]  J. Guerri,et al.  Genetic variability and evolutionary dynamics of viruses of the family Closteroviridae , 2013, Front. Microbiol..

[124]  C. Espinoza,et al.  Gene expression associated with compatible viral diseases in grapevine cultivars , 2007, Functional & Integrative Genomics.

[125]  M. Laimer,et al.  RESISTANCE TO VIRUSES, PHYTOPLASMAS AND THEIR VECTORS IN THE GRAPEVINE IN EUROPE: A REVIEW , 2009 .

[126]  S. Tatineni,et al.  A plant virus evolved by acquiring multiple nonconserved genes to extend its host range , 2011, Proceedings of the National Academy of Sciences.

[127]  O. Lemaire,et al.  Transmission of six ampeloviruses and two vitiviruses to grapevine by Phenacoccus aceris. , 2012, Phytopathology.

[128]  Suppress to Survive—Implication of Plant Viruses in PTGS , 2014, Plant Molecular Biology Reporter.

[129]  E. Ainsworth,et al.  Carbohydrate Export from the Leaf: A Highly Regulated Process and Target to Enhance Photosynthesis and Productivity , 2010, Plant Physiology.

[130]  S. Tatineni,et al.  Citrus tristeza virus-host interactions , 2013, Front. Microbiol..

[131]  V. Dolja Beet yellows virus: the importance of being different. , 2003, Molecular plant pathology.

[132]  Fei He,et al.  Biosynthesis of Anthocyanins and Their Regulation in Colored Grapes , 2010, Molecules.

[133]  P. Gross,et al.  Inflorescence of grapevine (Vitis vinifera L.): a high ability to distribute its own assimilates. , 2011, Journal of experimental botany.

[134]  R. Ayub,et al.  Fisiologia foliar e qualidade enológica da uva em videiras infectadas por vírus , 2010 .

[135]  Y. Gamalei Structure and function of leaf minor veins in trees and herbs , 1989, Trees.

[136]  M. Fuchs,et al.  Comparative Performance of Virus-Infected Vitis vinifera cv. Savagnin rose Grafted onto Three Rootstocks , 2010, American Journal of Enology and Viticulture.

[137]  J. Li,et al.  Complete nucleotide sequence of a Chinese isolate of Grapevine leafroll-associated virus 3 reveals a 5′ UTR of 802 nucleotides , 2013, Virus Genes.

[138]  R. Gutiérrez,et al.  Compatible GLRaV-3 viral infections affect berry ripening decreasing sugar accumulation and anthocyanin biosynthesis in Vitis vinifera , 2011, Plant Molecular Biology.

[139]  M. Heinlein,et al.  Manipulation of Plant Host Susceptibility: An Emerging Role for Viral Movement Proteins? , 2012, Front. Plant Sci..

[140]  R. Turgeon,et al.  A comprehensive picture of phloem loading strategies , 2009, Proceedings of the National Academy of Sciences.

[141]  M. Megraw,et al.  A comparative study of ripening among berries of the grape cluster reveals an altered transcriptional programme and enhanced ripening rate in delayed berries , 2014, Journal of experimental botany.